Soluble FMS-like Tyrosine Kinase 1 promotes angiotensin II sensitivity in preeclampsia

Journal of Clinical Investigation

Volumn 126, Issue 7, 2016, Pages 2561-2574

  Burke, Suzanne D ^a,b   Zsengellér, Zsuzsanna K ^a,c   Khankin, Eliyahu V ^a,b   Lo, Agnes S ^a,b   Rajakumar, Augustine ^a,b   DuPont, Jennifer J ^d   McCurley, Amy ^d   Moss, Mary E ^d,e   Zhang, Dongsheng ^a,b   Clark, Christopher D ^a,b   Wang, Alice ^a,b   Seely, Ellen W ^a,c   Kang, Peter M ^a,b   Stillman, Isaac E ^a,c   Jaffe, Iris Z ^d   Karumanchi, S Ananth ^a,b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c TUFTS MEDICAL CENTER   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN II; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; PHOSPHODIESTERASE V; PROTEIN TYROSINE KINASE; SILDENAFIL; SOLUBLE FMS LIKE TYROSINE KINASE 1; UNCLASSIFIED DRUG; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 1; ANGIOTENSIN DERIVATIVE; FLT1 PROTEIN, MOUSE;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; ENDOTHELIAL DYSFUNCTION; FEMALE; FETUS; FETUS OUTCOME; FETUS WEIGHT; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; MALE; MATERNAL HYPERTENSION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PLACENTA PERFUSION; PLACENTA TISSUE; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UTERINE VASCULAR RESISTANCE; UTERUS BLOOD FLOW; VASCULAR RESISTANCE; VASCULARIZATION; ANIMAL; BLOOD PRESSURE; BREEDING; CHEMISTRY; DISEASE MODEL; METABOLISM; PHOSPHORYLATION; PLACENTA; PREGNANCY; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

ANGIOTENSIN II; ANGIOTENSINS; ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PHOSPHORYLATION; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY, ANIMAL; SIGNAL TRANSDUCTION; SILDENAFIL CITRATE; TREATMENT OUTCOME; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84978420913     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83918     Document Type: Article

References (75)

1. Powe CE, Levine RJ, Karumanchi SA. Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors and implications for later cardiovascular disease. Circulation. 2011; 123 (24):2856-2869.
2. Redman CW, Sargent IL. Latest advances in understanding preeclampsia. Science. 2005; 308 (5728):1592-1594.
3. Gant NF, Daley GL, Chand S, Whalley PJ, MacDonald PC. A study of angiotensin II pressor response throughout primigravid pregnancy. J Clin Invest. 1973; 52 (11):2682-2689.
4. Chesley LC Vascular reactivity in normal and toxemic pregnancy. Clin Obstet Gynecol. 1966; 9 (4):871-881.
5. Chesley LC, Talledo E, Bohler CS, Zuspan FP. Vascular reactivity to angiotensin ii and norepinephrine in pregnant women. Am J Obstet Gynecol. 1965; 91:837-842.
6. Dekker GA, Makovitz JW, Wallenburg HC. Prediction of pregnancy-induced hypertensive disorders by angiotensin II sensitivity and supine pressor test. Br J Obstet Gynaecol. 1990; 97 (9):817-821.
7. Wallukat G, et al. Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J Clin Invest. 1999; 103 (7):945-952.
8. Wenzel K, et al. Angiotensin II type 1 receptor antibodies and increased angiotensin II sensitivity in pregnant rats. Hypertension. 2011; 58 (1):77-84.
9. AbdAlla S, Lother H, el Massiery A, Quitterer U. Increased AT1 receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med. 2001; 7 (9):1003-1009.
10. Quitterer U, Lother H, Abdalla S. AT1 receptor heterodimers and angiotensin II responsiveness in preeclampsia. Semin Nephrol. 2004; 24 (2):115-119.
11. Holobotovskyy V, et al. Regulator of G protein signaling 5 is a determinant of gestational hypertension and preeclampsia. Sci Transl Med. 2015; 7 (290):290ra88.
12. Alexander BT, Cockrell K, Cline FD, Llinas MT, Sedeek M, Granger JP. Effect of angiotensin II synthesis blockade on the hypertensive response to chronic reductions in uterine perfusion pressure in pregnant rats. Hypertension. 2001; 38 (3 Pt 2):742-745.
13. Shah DM Role of the renin-angiotensin system in the pathogenesis of preeclampsia. Am J Physiol Renal Physiol. 2005; 288 (4):F614-F625.
14. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A. 1993; 90 (22):10705-10709.
15. Chaiworapongsa T, et al. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med. 2005; 17 (1):3-18.
16. Chaiworapongsa T, et al. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol. 2004; 190 (6):1541-1547.
17. Levine RJ, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004; 350 (7):672-683.
18. Maynard SE, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003; 111 (5):649-658.
19. Venditti CC, Casselman R, Young I, Karumanchi SA, Smith GN. Carbon monoxide prevents hypertension and proteinuria in an adenovirus sFlt-1 preeclampsia-like mouse model. PLoS One. 2014; 9 (9):e106502.
20. Bergmann A, et al. Reduction of circulating soluble Flt-1 alleviates preeclampsia-like symptoms in a mouse model. J Cell Mol Med. 2010; 14 (6B):1857-1867.
21. Seligman SP, Buyon JP, Clancy RM, Young BK, Abramson SB. The role of nitric oxide in the pathogenesis of preeclampsia. Am J Obstet Gynecol. 1994; 171 (4):944-948.
22. Sandrim VC, Palei AC, Metzger IF, Gomes VA, Cavalli RC, Tanus-Santos JE. Nitric oxide formation is inversely related to serum levels of antiangiogenic factors soluble fms-like tyrosine kinase-1 and soluble endogline in preeclampsia. Hypertension. 2008; 52 (2):402-407.
23. Sessa WC eNOS at a glance. J Cell Sci. 2004; 117 (pt 12):2427-2429.
24. Kroll J, Waltenberger J. VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun. 1998; 252 (3):743-746.
25. Bussolati B, Dunk C, Grohman M, Kontos CD, Mason J, Ahmed A. Vascular endothelial growth factor receptor-1 modulates vascular endothelial growth factor-mediated angiogenesis via nitric oxide. Am J Pathol. 2001; 159 (3):993-1008.
26. Rafikov R, et al. eNOS activation and NO function: structural motifs responsible for the posttranslational control of endothelial nitric oxide synthase activity. J Endocrinol. 2011; 210 (3):271-284.
27. Kulandavelu S, Qu D, Adamson SL. Cardiovas-cular function in mice during normal pregnancy and in the absence of endothelial NO synthase. Hypertension. 2006; 47 (6):1175-1182.
28. Niu XF, Smith CW, Kubes P. Intracellular oxidative stress induced by nitric oxide synthesis inhibition increases endothelial cell adhesion to neutrophils. Circ Res. 1994; 74 (6):1133-1140.
29. Zhou XJ, Vaziri ND, Zhang J, Wang HW, Wang XQ. Association of renal injury with nitric oxide deficiency in aged SHR: prevention by hypertension control with AT1 blockade. Kidney Int. 2002; 62 (3):914-921.
30. von Dadelszen P, Ornstein MP, Bull SB, Logan AG, Koren G, Magee LA. Fall in mean arterial pressure and fetal growth restriction in pregnancy hypertension: a meta-analysis. Lancet. 2000; 355 (9198):87-92.
31. George EM, Palei AC, Dent EA, Granger JP. Sildenafil attenuates placental ischemia-induced hypertension. Am J Physiol Regul Integr Comp Physiol. 2013; 305 (4):R397-R403.
32. Herraiz S, et al. Sildenafil citrate improves perinatal outcome in fetuses from pre-eclamptic rats. BJOG. 2012; 119 (11):1394-1402.
33. Stanley JL, et al. Sildenafil citrate rescues fetal growth in the catechol-O-methyl transferase knockout mouse model. Hypertension. 2012; 59 (5):1021-1028.
34. Motta C, et al. Effect of sildenafil on pre-eclampsia-like mouse model induced By L-Name. Reprod Domest Anim. 2015; 50 (4):611-616.
35. March MI, et al. Circulating angiogenic factors and the risk of adverse outcomes among Haitian women with preeclampsia. PLoS One. 2015; 10 (5):e0126815.
36. Deng A, Engels K, Baylis C. Impact of nitric oxide deficiency on blood pressure and glomerular hemodynamic adaptations to pregnancy in the rat. Kidney Int. 1996; 50 (4):1132-1138.
37. Baylis C, Collins RC. Angiotensin II inhibition on blood pressure and renal hemodynamics in pregnant rats. Am J Physiol. 1986; 250 (2 Pt 2):F308-F314.
38. Baylis C. The determinants of renal hemodynamics in pregnancy. Am J Kidney Dis. 1987; 9 (4):260-264.
39. Robinson ES, et al. Suppression of the nitric oxide pathway in metastatic renal cell carcinoma patients receiving vascular endothelial growth factor-signaling inhibitors. Hypertension. 2010; 56 (6):1131-1136.
40. Gillis EE, Mooney JN, Garrett MR, Granger JP, Sasser JM. Sildenafil treatment ameliorates the maternal syndrome of preeclampsia and rescues fetal growth in the dahl salt-sensitive rat. Hypertension. 2016; 67 (3):647-653.
41. Bolnick JM, et al. Sildenafil stimulates human trophoblast invasion through nitric oxide and guanosine 3', 5'-cyclic monophosphate signaling. Fertil Steril. 2015; 103 (6):1587-1595.
42. Samangaya RA, et al. A randomised, doubleblinded, placebo-controlled study of the phosphodiesterase type 5 inhibitor sildenafil for the treatment of preeclampsia. Hypertens Pregnancy. 2009; 28 (4):369-382.
43. Krause BJ, Hanson MA, Casanello P. Role of nitric oxide in placental vascular development and function. Placenta. 2011; 32 (11):797-805.
44. Izumi H, Yallampalli C, Garfield RE. Gestational changes in L-arginine-induced relaxation of pregnant rat and human myometrial smooth muscle. Am J Obstet Gynecol. 1993; 169 (5):1327-1337.
45. Yallampalli C, Garfield RE, Byam-Smith M. Nitric oxide inhibits uterine contractility during pregnancy but not during delivery. Endocrinology. 1993; 133 (4):1899-1902.
46. Lowe DT Nitric oxide dysfunction in the pathophysiology of preeclampsia. Nitric Oxide. 2000; 4 (4):441-458.
47. Conrad KP, et al. Identification of increased nitric oxide biosynthesis during pregnancy in rats. FASEB J. 1993; 7 (6):566-571.
48. Fukumura D, et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci U S A. 2001; 98 (5):2604-2609.
49. Xue B, Singh M, Guo F, Hay M, Johnson AK. Protective actions of estrogen on angiotensin II-induced hypertension: role of central nitric oxide. Am J Physiol Heart Circ Physiol. 2009; 297 (5):H1638-H1646.
50. Li F, et al. eNOS deficiency acts through endothelin to aggravate sFlt-1-induced preeclampsia-like phenotype. J Am Soc Nephrol. 2012; 23 (4):652-660.
51. Ackermann A, Fernandez-Alfonso MS, Sanchez de Rojas R, Ortega T, Paul M, Gonzalez C. Modulation of angiotensin-converting enzyme by nitric oxide. Br J Pharmacol. 1998; 124 (2):291-298.
52. Loscalzo J. Nitric oxide insufficiency, platelet activation, and arterial thrombosis. Circ Res. 2001; 88 (8):756-762.
53. Kulandavelu S, Whiteley KJ, Qu D, Mu J, Bainbridge SA, Adamson SL. Endothelial nitric oxide synthase deficiency reduces uterine blood flow, spiral artery elongation, and placental oxygenation in pregnant mice. Hypertension. 2012; 60 (1):231-238.
54. Yallampalli C, Garfield RE. Inhibition of nitric oxide synthesis in rats during pregnancy produces signs similar to those of preeclampsia. Am J Obstet Gynecol. 1993; 169 (5):1316-1320.
55. Radi R. Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci U S A. 2004; 101 (12):4003-4008.
56. Rajagopalan S, et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest. 1996; 97 (8):1916-1923.
57. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res. 2000; 87 (10):840-844.
58. Li L, Pan Y, Dai L, Liu B, Zhang D. Association of genetic polymorphisms on vascular endothelial growth factor and its receptor genes with susceptibility to coronary heart disease. Med Sci Monit. 2016; 22:31-40.
59. Li W, Croce K, Steensma DP, McDermott DF, Ben-Yehuda O, Moslehi J. Vascular and metabolic implications of novel targeted cancer therapies: focus on kinase inhibitors. J Am Coll Cardiol. 2015; 66 (10):1160-1178.
60. Vigneau C, et al. All anti-vascular endothelial growth factor drugs can induce 'pre-eclampsia-like syndrome': a RARe study. Nephrol Dial Transplant. 2014; 29 (2):325-332.
61. Holwerda KM, et al. Hydrogen sulfide attenuates sFlt1-induced hypertension and renal damage by upregulating vascular endothelial growth factor. J Am Soc Nephrol. 2014; 25 (4):717-725.
62. Venkatesha S, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006; 12 (6):642-649.
63. August P, et al. Longitudinal study of the reninangiotensin-aldosterone system in hypertensive pregnant women: deviations related to the development of superimposed preeclampsia. Am J Obstet Gynecol. 1990; 163 (5 Pt 1):1612-1621.
64. Zhou CC, et al. Autoantibody from women with preeclampsia induces soluble Fms-like tyrosine kinase-1 production via angiotensin type 1 receptor and calcineurin/nuclear factor of activated T-cells signaling. Hypertension. 2008; 51 (4):1010-1019.
65. Irani RA, et al. The detrimental role of angioten-sin receptor agonistic autoantibodies in intrauterine growth restriction seen in preeclampsia. J Exp Med. 2009; 206 (12):2809-2822.
66. Dechend R, et al. AT1 receptor agonistic antibodies from preeclamptic patients stimulate NADPH oxidase. Circulation. 2003; 107 (12):1632-1639.
67. Chen CW, Jaffe IZ, Karumanchi SA. Preeclampsia and cardiovascular disease. Cardiovasc Res. 2014; 101 (4):579-586.
68. Pruthi D, et al. Exposure to experimental preeclampsia in mice enhances the vascular response to future injury. Hypertension. 2015; 65 (4):863-870.
69. Mandala M, Osol G. Physiological remodelling of the maternal uterine circulation during pregnancy. Basic Clin Pharmacol Toxicol. 2012; 110 (1):12-18.
70. Saxena AR, Karumanchi SA, Brown NJ, Royle CM, McElrath TF, Seely EW. Increased sensitivity to angiotensin II is present postpartum in women with a history of hypertensive pregnancy. Hypertension. 2010; 55 (5):1239-1245.
71. Hladunewich MA, et al. Postpartum assessment of the renin angiotensin system in women with previous severe, early-onset preeclampsia. J Clin Endocrinol Metab. 2011; 96 (11):3517-3524.
72. Mongraw-Chaffin ML, Cirillo PM, Cohn BA. Preeclampsia and cardiovascular disease death: prospective evidence from the child health and development studies cohort. Hypertension. 2010; 56 (1):166-171.
73. Li Z, et al. Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension. 2007; 50 (4):686-692.
74. Burke SD, et al. Spiral arterial remodeling is not essential for normal blood pressure regulation in pregnant mice. Hypertension. 2010; 55 (3):729-737.
75. Rajakumar A, et al. Transcriptionally active syncytial aggregates in the maternal circulation may contribute to circulating soluble fms-like tyrosine kinase 1 in preeclampsia. Hypertension. 2012; 59 (2):256-264.